Skip to main content
SpringerLink
Log in

Potassium transport across the frog retinal pigment epithelium

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Previous experiments indicate that the apical membrane of the frog retinal pigment epithelium contains electrogenic Na∶K pumps. In the pressent experiments net potassium and rubidium transport across the epithelium was measured as a function of extracellular potassium (rubidium) concentration, [K] o ([Rb] o ). The net rate of retina-to-choroid42K(86Rb) transport increased monotonically as [K] o ([Rb] o ), increased from approximately 0.2 to 5mm on both sides of the tissue or on the apical (neural retinal) side of the tissue. No further increase was observed when [K] o ([Rb] o ) was elevated to 10mm. Net sodium transport was also stimulated by elevating [K] o . The net K transport was completely inhibited by 10−4 m ouabain in the solution bathing the apical membrane. Ouabain inhibited the unidirectional K flux in the direction of net flux but had not effect on the back-flux in the choroid-to-retina direction. The magnitude of the ouabain-inhibitable42K(86Rb) flux increased with [K] o ([Rb] o ). These results show that the apical membrane Na∶K pumps play an important role in the net active transport of potassium (rubidium) across the epithelium. The [K] o changes that modulate potassium transport coincide with the light-induced [K] o changes that occur in the extracellular space separating the photoreceptors and the apical membrane of the pigment epithelium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abercrombie, R.F., DeWeer, P. 1978. Electric current generated by squid giant axon sodium pump: External K and internal ADP effects.Am. J. Physiol. 235(1):C63-C68

    PubMed  Google Scholar 

  • Armstrong, W.McD., Garcia-Diaz, J.F., O'Dougherty, J., O'Regan, M. 1979. Transmural Na+ electrochemical potential difference and sodium accumulation in epithelial cells of the small intestine.Fed. Proc. 38:2722–2728

    PubMed  Google Scholar 

  • Baker, P.F., Blaustein, M.P., Keynes, R.D., Manil, J., Shaw, I.T., Steinhardt, R.A. 1969. The ouabain-sensitive fluxes of sodium and potassium in squid giant axons.J. Physiol. (London) 200:459–496

    Google Scholar 

  • Bok, D. 1980. Autoradiographic studies on the polarity of plasma membrane receptors in the retinal pigment epithelium cells. IV. International Symposium on the Structure of the Eye. J. Hollyfield, editor. Elsevier-North Holland (in press)

  • Cala, P.M., Cogswell, N., Mandel, L.J. 1978. Binding or3H ouabain to split frog skin.J. Gen. Physiol. 71:347–367

    PubMed  Google Scholar 

  • Capovilla, M., Cervetto, L., Torre, V. 1980. Effects of changing external potassium and chloride concentrations on the photoresponses ofBufo Bufo rods.J. Physiol. (London) 307:529–551

    Google Scholar 

  • Cavaggioni, A., Sorbi, R.T., Turini, S. 1973. Efflux of potassium from isolated rod outer segments: A photic effect.J. Physiol. (London) 232:609–620

    Google Scholar 

  • Dawson, D.C. 1977. Tracer flux ratios: A phenomenological approach.J. Membrane Biol. 31:351–358

    Google Scholar 

  • Faber, D.S. 1969. Analysis of the slow transretinal potentials in response to light. Ph.D. Thesis, State University of New York at Buffalo, New York

    Google Scholar 

  • Garay, R.P., Garrahan, P.J. 1973. The interaction of sodium and potassium with the sodium pump in red cells.J. Physiol. (London) 231:297–325

    Google Scholar 

  • Ginsburg, B.F., Hogg, J. 1967. What does a short-circuit current measure in biological systems?J Theor. Biol. 14:316–322

    Google Scholar 

  • Henderson, E.C. 1974. Strophanthidim sensitive electrogenic mechanisms in frog sartorius muscles exposed to barium.Pfluegers Arch. 350:81–95

    Google Scholar 

  • Hermsmeyer, K., Sperelakis, N. 1970. Decrease in K+-conductance and depolarization of frog cardiac muscle produced by Ba++.Am J. Physiol. 219:1108–1114

    PubMed  Google Scholar 

  • Hodgkin, A.L., Horowicz, P. 1959. The influence of potassium and chloride ions on the membrane potential of single muscle fibers.J. Physiol. (London) 148:127–160

    Google Scholar 

  • Hoffman, J.F., Kaplan, J.H., Callahan, T.J. 1979. The Na∶K pump in red cells is electrogenic.Fed. Proc. 38:2440–2441

    PubMed  Google Scholar 

  • Hudspeth, A.J., Yee, A.G. 1973. The intercellular junctional complexes of retinal pigment epithelia.Invest. Ophthal. 12:354–365

    PubMed  Google Scholar 

  • Joiner, C.H., Lauf, P.L. 1978. Modulation of ouabain binding and potassium pump fluxes by cellular sodium and potassium in human and sheep erythrocytes.J. Physiol. (London) 283:177–196

    Google Scholar 

  • Kennedy, B.G., DeWeer, P. 1977a. Strophanthidan-sensitive sodium fluxes in metabolically poisoned frog skeletal muscle.J. Gen. Physiol. 68:405–420

    Google Scholar 

  • Kennedy, B.G., DeWeer, P. 1977b. Relationship between Na∶K and Na∶Na exchange by the sodium pump of skeletal muscle.Nature (London) 268:165–167

    Google Scholar 

  • Knight, A.B., Welt, L.G. 1974. Intracellular potassium: A determinant of the sodium-potassium pump rate.J. Gen. Physiol. 63:351–373

    PubMed  Google Scholar 

  • Lewis, S.A., Wills, K. 1979. Intracellular ion activities and their relationship to membrane properties of tight epithelia.Fed. Proc. 38:2739–2742

    PubMed  Google Scholar 

  • Lipton, S.A., Ostroy, S.E., Dowling, J.E. 1977. Electrical and adaptive properties of rod photoreceptors inBufo marinus.J. Gen. Physiol. 70:747–770

    PubMed  Google Scholar 

  • Matsuura, T., Miller, W.H., Tomita, T. 1978. Cone-specificc-wave in the turtle retina.Vis. Res. 18:767–775

    PubMed  Google Scholar 

  • Miller, S.S., Steinberg, R.H. 1977a. Active transport of ions across frog retinal pigment epithelium.Exp. Eye. Res. 25:235–248

    PubMed  Google Scholar 

  • Miller, S.S., Steinberg, R.H. 1977b. Passive ionic properties of frog retinal pigment epithelium.J. Membrane Biol. 36:337–372

    Google Scholar 

  • Miller, S.S., Steinberg, R.H. 1979. Potassium modulation of taurine transport across the frog retinal pigment epithelium.J. Gen. Physiol. 74:237–259

    PubMed  Google Scholar 

  • Miller, S.S., Steinberg, R.H., Oakley, B., II. 1978. The electrogenic sodium pump of the frog retinal pigment epithelium.J. Membrane Biol. 44:259–279

    Google Scholar 

  • Moore, J.W., Anderson, N., Blaustein, M., Takata, M., Lettvin, J.Y., Pickard, W.F., Bernstein, T., Pooler, J. 1967. Alkali cation selectivity of squid axon membrane.Ann. N.Y. Acad. Sci. 137(2):818–829

    Google Scholar 

  • Nagel, W. 1979. Inhibition of potassium conductance by barium in frog skin epithelium.Biochim. Biophys. Acta 552:346–357

    PubMed  Google Scholar 

  • Nielsen, R. 1979. Coupled transepithelial sodium and potassium transport across isolated frog skin: Effect of ouabian, amiloride, and the polene antibiotic filipin.J. Membrane Biol. 57:161–184

    Google Scholar 

  • Nilsson, S.E.G. 1964. An electron microscopic classification of the retinal receptors of the leopard frog (Rana pipiens).J. Ultrastruct. Res. 10:390–416

    PubMed  Google Scholar 

  • Oakley, B., II. 1977. Potassium and the photoreceptor-dependent pigment epithelial hyperpolarization.J. Gen. Physiol. 70:405–425

    PubMed  Google Scholar 

  • Oakley, B., II, Flaming, D.G., Brown, K.T. 1979. Effects of the rod receptor potential upon extracellular potassium ion concentration.J. Gen. Physiol. 74:713–737

    PubMed  Google Scholar 

  • Oakley, B., II, Green, D.G. 1976. Correlation of light-induced changes in retinal extracellular potassium concentration withc-wave of the electroretinogram.J. Neurophysiol. 39:1117–1133

    PubMed  Google Scholar 

  • Oakley, B., II, Miller, S.S., Steinberg, R.H. 1978. Effects of intracellular potassium upon the electrogenic pump of frog retinal pigment epithelium.J. Membrane Biol. 44:281–307

    Google Scholar 

  • Oakley, B., II, Steinberg, R.H. 1981. Effects of maintained illumination upon [K] o in the subretinal space of the frog retina.Vis. Res. (in press)

  • Ogden, T.E., Ito, H. 1971. Avian retina. II. An evaluation of retinal electrical anisotropy.J. Neurophysiol. 34:367–373

    PubMed  Google Scholar 

  • Ostwald, T., Steinberg, R.H. 1980. Localization of frog retinal pigment epithelium (Na, K)-ATPase.Exp. Eye Res. 31:351–360

    PubMed  Google Scholar 

  • Porter, K.R., Yamada, E. 1960. Studies on the endoplasmic reticulum. V. Its form and differentiation in pigment epithelial cells of the frog retina.J. Biophys. Biochem. Cytol. 8:181–205

    PubMed  Google Scholar 

  • Reuss, L., Weinman, S.A. 1979. Intracellular ionic activities and transmembrane electrochemical potential differences in gall bladder epithelium.J. Membrane Biol. 49:345–362

    Google Scholar 

  • Rick, R.A., Dorge, E., Arnim, E. von, Thurau, K. 1978. Electron microprobe analysis of frog skin epithelium. Evidence for a syncytial sodium transport compartment.J. Membrane Biol. 39:313–331

    Google Scholar 

  • Riley, M.V., Winkler, B.S., Benner, J., Yates, E.M. 1978. ATPase activities in retinal pigment epithelium and choroid.Exp. Eye Res. 26:445–455

    PubMed  Google Scholar 

  • Simons, T.J.B. 1974. Potassium: potassium exchange catalysed by the sodium pump in human red cells.J. Physiol. (London) 237:123–155

    Google Scholar 

  • Sjodin, R.A. 1959. Rubidium and cesium fluxes in muscle as related to the membrane potential.J. Gen. Physiol. 42:983–1003

    PubMed  Google Scholar 

  • Spring, K.R., Kimura, G. 1979. Intracellular ionic activities inNecturus proximal tubule.Fed. Proc. 38:2729–2732

    PubMed  Google Scholar 

  • Standen, N.B., Stanfield, P.R. 1980. Rubidium block and rubidium permeability of the inward rectifier of frog skeletal muscle fibers.J. Physiol. (London) 304:415–435

    Google Scholar 

  • Steinberg, R.H. 1973. Scanning electron microscopy of the bullfrog's retina and pigment epithelium.Z. Zellforsch. 143:451–463

    PubMed  Google Scholar 

  • Steinberg, R.H., Miller, S. 1973. Aspects of electrolyte transport in frog pigment epithelium.Exp. Eye Res. 16:365–372

    PubMed  Google Scholar 

  • Steinberg, R.H., Miller, S.S. 1979. Transport and membrane properties of the retinal pigment epithelium.In: The Retinal Pigment Epithelium. K.M. Zinn and M.F. Marmor, editors. pp. 205–225. Harvard University Press, Cambridge, Mass.

    Google Scholar 

  • Steinberg, R.H., Oakley, B., II, Niemeyer, G. 1980. Light-evoked changes in [K+] o in the retina of the intact cat eye.J. Neurophysiol. 44:897–921

    PubMed  Google Scholar 

  • Thomas, R.C. 1972. Electrogenic sodium pump in nerve and muscle cells.Physiol. Rev. 52:463–594

    Google Scholar 

  • Wright, E.M. 1972. Mechanisms of ion transport across the choroid plexus.J. Physiol. (London) 226:545–571

    Google Scholar 

  • Zeuthen, T. 1978. Intracellular gradients of ion activities in the epithelial cells of theNecturus gall bladder recorded with ion-selective microelectrodes.J. Membrane Biol. 39:185–218

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Optometry, University of California, 94720, Berkeley, California

    Sheldon S. Miller & Roy H. Steinberg

  2. Departments of Physiology and Ophthalmology, University of California, San Francisco, California

    Sheldon S. Miller & Roy H. Steinberg

Authors
  1. Sheldon S. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roy H. Steinberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miller, S.S., Steinberg, R.H. Potassium transport across the frog retinal pigment epithelium. J. Membrain Biol. 67, 199–209 (1982). https://doi.org/10.1007/BF01868661

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01868661

Key words

Search

Navigation